Neuroelectrical imaging study of music perception by children with unilateral and bilateral cochlear implants Pasquale Marsella 1, Alessandro Scorpecci 1, Giovanni Vecchiato 2, Alfredo Colosimo 3, Anton Giulio Maglione 3, Fabio Babiloni 2,4 Department of Otorhinolaryngology, Audiology and Otology Unit, “Bambino Gesù” Pediatric Hospital, Rome, Italy, 2Department of Physiology and Pharmacology, University of Rome “Sapienza”, Italy, 3Department of Anatomy, Histology, Forensic Medicine and Orthopedics, University of Rome “Sapienza”, Italy, 4Neuroelectrical Imaging and BCI lab, IRCCS Fondazione Santa Lucia, Italy 1
Objective: To investigate by means of non-invasive neuroelectrical imaging the differences in the perceived pleasantness of music between children with cochlear implants (CI) and normal-hearing (NH) children. Methods: 5 NH children and 5 children who received a sequential bilateral CI were assessed by means of High-Resolution EEG with Source Reconstruction as they watched a musical cartoon. Implanted children were tested before and after the second implant. For each subject the scalp Power Spectral Density was calculated in order to investigate the EEG alpha asymmetry. Results: The scalp topographic distribution of the EEG power spectrum in the alpha band was different in children using one CI as compared to NH children (see figure). With two CIs the cortical activation pattern changed significantly, becoming more similar to the one observed in NH children. Conclusions: The findings support the hypothesis that bilateral CI users have a closer-to-normal perception of the pleasantness of music than unilaterally implanted children. Keywords: Cochlear implant, Children, Bilateral, Music, Brain, EEG
Introduction Most cochlear implant (CI) users report difficulties with music perception even after many years of implant use (Gfeller et al., 2000; McDermott, 2004; Galvin et al., 2007; Veekmans et al., 2009). Like adult CI recipients, children show difficulties in simple melody and song recognition tasks (Vongpaisal et al., 2006; Mitani et al., 2007), but unlike adults they seem to enjoy music listening and are often engaged in musical activities both in school and in leisure time. Such a discrepancy can be explained by considering that beyond the objective characteristics of sounds, the emotional and affective component is also very important in the experience of listening to music, and possibly so important as to be the predominant element underlying music appreciation by child CI recipients (Volkova et al. 2013). With this in mind, an objective assessment of the perceived pleasantness of musical stimuli would be a valuable tool to investigate the degree of music appreciation by child CI users. Correspondence to: Pasquale Marsella, Audiology and Otology Unit, Bambino Gesù Pediatric Hospital, Piazza S. Onofrio 4, 00165, Rome. E-mail: [email protected]
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Over the last decades, the variations of the activity of certain cortical areas have been put in strict correlation with the pleasantness of an individual’s experienced perception. Such areas include the pre-frontal and the frontal cortex (PFC and FC, respectively) (Davidson and Irwin, 1999). The PFC region is structurally and functionally heterogeneous, but its role in the generation of emotions is well recognized (Davidson, 2002). Electroencephalogram (EEG) spectral power analyses indicate that the anterior cerebral hemispheres are differentially lateralized for approach and withdrawal motivational tendencies and emotions. Specifically, the findings suggest that the left PFC is an important brain area in a widespread circuit that mediates an appetitive approach, whereas the right PFC appears to form a major component of a neural circuit underlying defensive withdrawal (Davidson, 2000, 2004). To date, no studies in the literature have investigated whether bilateral CI affords a more pleasant perception of music than unilateral CI in pediatric subjects. This study hypothesizes that by providing a more symmetrical cortical activation (Gordon et al., 2013) bilateral CI should also provide an increased pleasantness of music perception by deaf children.
Cochlear Implants International
2014
VOL.
15
NO.
S1
Marsella et al.
Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Therefore, the aims of the study are to investigate, by means of high-resolution EEG with source reconstruction:
video and no sound (MUTE condition). Professional software for audio manipulation was used.
• the differences in the perceived pleasantness of music between children with CIs and normal-hearing (NH) children. • in the CI group, the changes in the cortical activation elicited by music before and after sequential cochlear implantation.
EEG recordings
Methods Population Five NH children and five unilaterally implanted children who were candidates for sequential, bilateral CI were enrolled. Mean age was 43 ± 7.4 months for the NH group and 41.5 ± 6.9 months for the CI group. Gender distribution was three female and two male for both groups. All implanted children were using a Nucleus CP810 processor with 25 μs pulse width, 900 pps stimulation rate and ACE strategy. On the day the registration was performed, they received warble-tone free-field audiometry and speech audiometry to make sure their hearing and speech recognition abilities were good. All children were assessed by high-resolution EEG with source reconstruction as they were watching a musical cartoon. NH children were assessed once, implanted children twice: with one CI before sequential bilateral CI surgery and with two CIs after at least 3 months of second CI use.
Stimuli Audiovisual stimuli consisted of a 4-minute piece of the cartoon Fantasia accompanied by the original music by D. Paradisi. Such a stimulus was chosen because music plays an important role in cartoon films. Three versions of the videoclip were delivered to each subject in a random order: the original video plus the original music (NORMAL condition); the original video and a distorted and unpleasant version of the music, obtained by reversing the audio flow and changing the pitch and the interval of the original music (DISTORT condition); the original
Figure 1
Photograph depicting test conditions.
During EEG data acquisition, all the subjects were comfortably sitting on a chair, in an electrically shielded, dimly lit room. A 64-channel EEG system (BEPlus, EBNeuro spa, Italy) at a sampling rate of 256 Hz was used to record electrical potentials by means of an electrode cap, according to an extension of the 10–20 international system (Fig. 1). Since a clear role of the frontal areas has been depicted for the investigated phenomena (Davidson, 2002, 2004; Davidson and Irwin, 1999), we used the left and right frontal and prefrontal electrodes of the 10–20 international system to compute the spectral analysis. The following channels were considered: Af7, Af8, F3, Fz, F4, T7, C3, Cz, C4, T8, P3, Pz, P4, O1, O2. The EEG signals were band pass filtered at 1–45 Hz and purified of ocular artifacts by employing the Independent Component Analysis (ICA). The recording sessions were segmented in order to analyze the EEG activity elicited during the NORMAL, DISTORT, and MUTE conditions. The EEG traces related to our datasets of interest were further segmented in to several EEG trials with a length of one second each. Later, a semi-automatic procedure was adopted to reject trials presenting muscular and other kinds of movement artifacts. Only artifact-free trials were considered for the analysis. Individual alpha frequency was calculated for each subject in order to define our band of interest according to the method suggested in the scientific literature (Klimesch, 1999).
Estimation of cortical activity Cortical activity from EEG scalp recordings was estimated by using a realistic head model, consisting of about 4000 dipoles uniformly located on the cortical surface. The estimation of the power spectral density (PSD) in the alpha band and several regions of interest (ROIs), according to Brodmann areas, was made in accordance with the Welch procedure. The statistical significance of the power spectral values during the observation of the different experimental conditions analyzed was assessed by cortical maps, for each subject. The PSD for each ROI, in different conditions, has been compared using Student’s t-test, false discovery rate corrected for multiple comparisons (P < 0.05). The results are presented on a realistic head model (Colin template, from McGill University). In particular, the average brain model was used to display the cortical areas that show statistically significant activation during the different experimental conditions in the study subjects. Hence, ROIs of the average brain model were highlighted in red (blue) if subjects
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Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Figure 2 Statistical cortical map in the alpha band comparing NORMAL and DISTORT conditions in normalhearing (left) and unilaterally implanted (right) subjects. In both panels, the color bar ranges from red to blue indicating the cortical regions in which there is a statistically significant increase in alpha activity during the presentation of the normal (distorted) video clip at 5% significance (Bonferroni corrected, as the symbol * indicates). Frontal (top) and lateral (bottom) views of the map are shown.
showed a statistically significant increase of PSD for the DISTORT (MUTE) condition. The intensity of the color codes the number of subjects presenting the activation. Gray color indicates no statistical difference in the analyzed populations.
Results Fig. 2 shows the differences in average cortical activation between the NH and the Unilateral CI group in the NORMAL vs. DISTORT comparison: the areas of red activity clearly visible on the NH right prefrontal cortex indicate that in the prefrontal right areas there is a better synchronization of the alpha rhythm during the observation of the NORMAL videoclip than during the observation of the videoclip with the dissonant sound (DISTORT). Because alpha desynchronization is associated with a ‘rest’ condition,
Figure 3 Statistical cortical map in the alpha band comparing NORMAL and MUTE conditions in normal-hearing (left) and unilaterally implanted (right) subjects. In both panels, the color bar ranges from red to blue indicating the cortical regions in which there is a statistically significant increase in alpha activity during the presentation of the normal (mute) video clip at 5% significance (Bonferroni corrected, as the symbol * indicates). Frontal (top) and lateral (bottom) views of the map are shown.
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this means that the right prefrontal cortex (repulsion from a stimulus) of NH children is more at rest at delivery of NORMAL music, and thus automatically less at rest (i.e. more engaged) at the delivery of DISTORT music. These results are consistent with the common notion that NH children dislike distorted music. In the CI group, the activation pattern seems to be the opposite: the areas of blue activity in the right prefrontal cortex (repulsion from a stimulus) suggest that in this population alpha synchronization occurs to a greater extent at presentation of the DISTORT condition. This in turn indicates dislike for NORMAL music. When the NORMAL and MUTE conditions are compared (Fig. 3), once again NH subjects seem consistent with Davidson’s withdrawal/approach theory: they show greater alpha synchronization of the right prefrontal cortex for NORMAL music (blue), which implies greater desynchronization (i.e. repulsion, dislike) with the MUTE condition. In contrast, unilateral CI children show the very opposite pattern of cortical activation: they present a greater alpha synchronization in the right prefrontal cortex in the MUTE condition (red), which means greater alpha desynchronization (i.e. repulsion, dislike) in the NORMAL condition. In contrast, the results obtained in the CI group after 3 months’ use of the 2nd CI show, in the NORMAL vs. DISTORT comparison, a cortical activation pattern which resembles more closely the one observed in the NH subjects. Similarly, the cortical activation pattern observed in the bilaterally implanted subjects in the NORMAL vs. MUTE comparison is more similar to the one found in NH children.
Conclusions The results of this study confirm that in NH children the cortical activation in response to musical stimuli is consistent with the Davidson’s approach/withdrawal theory. More importantly, they indicate that unilaterally implanted subjects do not distinguish normal from distorted music in terms of increased/ decreased pleasantness of perceived stimuli. Such a difference may be due both to the peculiar cortical reorganization in prelingually deaf subjects and to an asymmetrical pattern of cortical activation consequential to unilateral CI stimulation. The latter hypothesis seems supported by the finding that sequential, bilateral CI restores a cortical activation pattern which resembles more closely the one observed in the NH group.
References Davidson R.J. 2000. Affective style, psychopathology, and resilience: brain mechanisms and plasticity. American Psychology, 55: 1196–11214. Davidson R.J. 2002. Anxiety and affective style: role of prefrontal cortex and amygdala. Biological Psychiatry 51: 68–80.
Marsella et al.
Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Davidson R.J. 2004. What does the prefrontal cortex “do” in affect: perspectives on frontal EEG asymmetry research. Biological Psychology, 67: 219–233. Davidson R.J., Irwin W. 1999. The functional neuroanatomy of emotion and affective style. Trends Cognition Science, 3: 11–21. Galvin J.J.I., Fu Q.J., Nogaki G. 2007. Melodic contour identification by cochlear implant listeners. Ear and Hearing, 28: 302–319. Gfeller K., Christ A., Knutson J.F., Witt S., Murray K.T., Tyler R.S. 2000. Musical backgrounds, listening habits, and aesthetic enjoyment of adult cochlear implant recipients. Journal of American Academy of Audiology, 11: 390–406. Gordon K.A., Wong D.D., Papsin B.C. 2013. Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf. Brain, 136: 1609–1625. Klimesch W. 1999. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Research. Brain Research Review, 29: 169–195.
McDermott H.J. 2004. Music perception with cochlear implants: a review. Trends Amplification, 8: 49–82. Mitani C., Nakata T., Trehub S.E., Kanda Y., Kumagami H., Takasaki K., et al. 2007. Music recognition, music listening, and word recognition by deaf children with cochlear implants. Ear and Hearing, 28(2 Suppl): 29S–33S. Veekmans K., Ressel L., Mueller J., Vischer M., Brockmeier S.J. 2009. Comparison of music perception in bilateral and unilateral cochlear implant users and normal hearing subjects. Audiology and Neurootology, 14: 315–326. Volkova A., Trehub S.E., Schellenberg E.G., Papsin B.C., Gordon K.A. 2013. Children with bilateral cochlear implants identify emotion in speech and music. Cochlear Implants International, 14: 80–91. Vongpaisal T., Trehub S.E., Schellenberg E.G. 2006. Song recognition by children and adolescents with cochlear implants. Journal of Speech Language Hearing Research, 49: 1091–1103.
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2014
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Objective: To investigate by means of non-invasive neuroelectrical imaging the differences in the perceived pleasantness of music between children with cochlear implants (CI) and normal-hearing (NH) children. Methods: 5 NH children and 5 children who received a sequential bilateral CI were assessed by means of High-Resolution EEG with Source Reconstruction as they watched a musical cartoon. Implanted children were tested before and after the second implant. For each subject the scalp Power Spectral Density was calculated in order to investigate the EEG alpha asymmetry. Results: The scalp topographic distribution of the EEG power spectrum in the alpha band was different in children using one CI as compared to NH children (see figure). With two CIs the cortical activation pattern changed significantly, becoming more similar to the one observed in NH children. Conclusions: The findings support the hypothesis that bilateral CI users have a closer-to-normal perception of the pleasantness of music than unilaterally implanted children. Keywords: Cochlear implant, Children, Bilateral, Music, Brain, EEG
Introduction Most cochlear implant (CI) users report difficulties with music perception even after many years of implant use (Gfeller et al., 2000; McDermott, 2004; Galvin et al., 2007; Veekmans et al., 2009). Like adult CI recipients, children show difficulties in simple melody and song recognition tasks (Vongpaisal et al., 2006; Mitani et al., 2007), but unlike adults they seem to enjoy music listening and are often engaged in musical activities both in school and in leisure time. Such a discrepancy can be explained by considering that beyond the objective characteristics of sounds, the emotional and affective component is also very important in the experience of listening to music, and possibly so important as to be the predominant element underlying music appreciation by child CI recipients (Volkova et al. 2013). With this in mind, an objective assessment of the perceived pleasantness of musical stimuli would be a valuable tool to investigate the degree of music appreciation by child CI users. Correspondence to: Pasquale Marsella, Audiology and Otology Unit, Bambino Gesù Pediatric Hospital, Piazza S. Onofrio 4, 00165, Rome. E-mail: [email protected]
S68
© W. S. Maney & Son Ltd 2014 DOI 10.1179/1467010014Z.000000000171
Over the last decades, the variations of the activity of certain cortical areas have been put in strict correlation with the pleasantness of an individual’s experienced perception. Such areas include the pre-frontal and the frontal cortex (PFC and FC, respectively) (Davidson and Irwin, 1999). The PFC region is structurally and functionally heterogeneous, but its role in the generation of emotions is well recognized (Davidson, 2002). Electroencephalogram (EEG) spectral power analyses indicate that the anterior cerebral hemispheres are differentially lateralized for approach and withdrawal motivational tendencies and emotions. Specifically, the findings suggest that the left PFC is an important brain area in a widespread circuit that mediates an appetitive approach, whereas the right PFC appears to form a major component of a neural circuit underlying defensive withdrawal (Davidson, 2000, 2004). To date, no studies in the literature have investigated whether bilateral CI affords a more pleasant perception of music than unilateral CI in pediatric subjects. This study hypothesizes that by providing a more symmetrical cortical activation (Gordon et al., 2013) bilateral CI should also provide an increased pleasantness of music perception by deaf children.
Cochlear Implants International
2014
VOL.
15
NO.
S1
Marsella et al.
Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Therefore, the aims of the study are to investigate, by means of high-resolution EEG with source reconstruction:
video and no sound (MUTE condition). Professional software for audio manipulation was used.
• the differences in the perceived pleasantness of music between children with CIs and normal-hearing (NH) children. • in the CI group, the changes in the cortical activation elicited by music before and after sequential cochlear implantation.
EEG recordings
Methods Population Five NH children and five unilaterally implanted children who were candidates for sequential, bilateral CI were enrolled. Mean age was 43 ± 7.4 months for the NH group and 41.5 ± 6.9 months for the CI group. Gender distribution was three female and two male for both groups. All implanted children were using a Nucleus CP810 processor with 25 μs pulse width, 900 pps stimulation rate and ACE strategy. On the day the registration was performed, they received warble-tone free-field audiometry and speech audiometry to make sure their hearing and speech recognition abilities were good. All children were assessed by high-resolution EEG with source reconstruction as they were watching a musical cartoon. NH children were assessed once, implanted children twice: with one CI before sequential bilateral CI surgery and with two CIs after at least 3 months of second CI use.
Stimuli Audiovisual stimuli consisted of a 4-minute piece of the cartoon Fantasia accompanied by the original music by D. Paradisi. Such a stimulus was chosen because music plays an important role in cartoon films. Three versions of the videoclip were delivered to each subject in a random order: the original video plus the original music (NORMAL condition); the original video and a distorted and unpleasant version of the music, obtained by reversing the audio flow and changing the pitch and the interval of the original music (DISTORT condition); the original
Figure 1
Photograph depicting test conditions.
During EEG data acquisition, all the subjects were comfortably sitting on a chair, in an electrically shielded, dimly lit room. A 64-channel EEG system (BEPlus, EBNeuro spa, Italy) at a sampling rate of 256 Hz was used to record electrical potentials by means of an electrode cap, according to an extension of the 10–20 international system (Fig. 1). Since a clear role of the frontal areas has been depicted for the investigated phenomena (Davidson, 2002, 2004; Davidson and Irwin, 1999), we used the left and right frontal and prefrontal electrodes of the 10–20 international system to compute the spectral analysis. The following channels were considered: Af7, Af8, F3, Fz, F4, T7, C3, Cz, C4, T8, P3, Pz, P4, O1, O2. The EEG signals were band pass filtered at 1–45 Hz and purified of ocular artifacts by employing the Independent Component Analysis (ICA). The recording sessions were segmented in order to analyze the EEG activity elicited during the NORMAL, DISTORT, and MUTE conditions. The EEG traces related to our datasets of interest were further segmented in to several EEG trials with a length of one second each. Later, a semi-automatic procedure was adopted to reject trials presenting muscular and other kinds of movement artifacts. Only artifact-free trials were considered for the analysis. Individual alpha frequency was calculated for each subject in order to define our band of interest according to the method suggested in the scientific literature (Klimesch, 1999).
Estimation of cortical activity Cortical activity from EEG scalp recordings was estimated by using a realistic head model, consisting of about 4000 dipoles uniformly located on the cortical surface. The estimation of the power spectral density (PSD) in the alpha band and several regions of interest (ROIs), according to Brodmann areas, was made in accordance with the Welch procedure. The statistical significance of the power spectral values during the observation of the different experimental conditions analyzed was assessed by cortical maps, for each subject. The PSD for each ROI, in different conditions, has been compared using Student’s t-test, false discovery rate corrected for multiple comparisons (P < 0.05). The results are presented on a realistic head model (Colin template, from McGill University). In particular, the average brain model was used to display the cortical areas that show statistically significant activation during the different experimental conditions in the study subjects. Hence, ROIs of the average brain model were highlighted in red (blue) if subjects
Cochlear Implants International
2014
VOL.
15
NO.
S1
S69
Marsella et al.
Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Figure 2 Statistical cortical map in the alpha band comparing NORMAL and DISTORT conditions in normalhearing (left) and unilaterally implanted (right) subjects. In both panels, the color bar ranges from red to blue indicating the cortical regions in which there is a statistically significant increase in alpha activity during the presentation of the normal (distorted) video clip at 5% significance (Bonferroni corrected, as the symbol * indicates). Frontal (top) and lateral (bottom) views of the map are shown.
showed a statistically significant increase of PSD for the DISTORT (MUTE) condition. The intensity of the color codes the number of subjects presenting the activation. Gray color indicates no statistical difference in the analyzed populations.
Results Fig. 2 shows the differences in average cortical activation between the NH and the Unilateral CI group in the NORMAL vs. DISTORT comparison: the areas of red activity clearly visible on the NH right prefrontal cortex indicate that in the prefrontal right areas there is a better synchronization of the alpha rhythm during the observation of the NORMAL videoclip than during the observation of the videoclip with the dissonant sound (DISTORT). Because alpha desynchronization is associated with a ‘rest’ condition,
Figure 3 Statistical cortical map in the alpha band comparing NORMAL and MUTE conditions in normal-hearing (left) and unilaterally implanted (right) subjects. In both panels, the color bar ranges from red to blue indicating the cortical regions in which there is a statistically significant increase in alpha activity during the presentation of the normal (mute) video clip at 5% significance (Bonferroni corrected, as the symbol * indicates). Frontal (top) and lateral (bottom) views of the map are shown.
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this means that the right prefrontal cortex (repulsion from a stimulus) of NH children is more at rest at delivery of NORMAL music, and thus automatically less at rest (i.e. more engaged) at the delivery of DISTORT music. These results are consistent with the common notion that NH children dislike distorted music. In the CI group, the activation pattern seems to be the opposite: the areas of blue activity in the right prefrontal cortex (repulsion from a stimulus) suggest that in this population alpha synchronization occurs to a greater extent at presentation of the DISTORT condition. This in turn indicates dislike for NORMAL music. When the NORMAL and MUTE conditions are compared (Fig. 3), once again NH subjects seem consistent with Davidson’s withdrawal/approach theory: they show greater alpha synchronization of the right prefrontal cortex for NORMAL music (blue), which implies greater desynchronization (i.e. repulsion, dislike) with the MUTE condition. In contrast, unilateral CI children show the very opposite pattern of cortical activation: they present a greater alpha synchronization in the right prefrontal cortex in the MUTE condition (red), which means greater alpha desynchronization (i.e. repulsion, dislike) in the NORMAL condition. In contrast, the results obtained in the CI group after 3 months’ use of the 2nd CI show, in the NORMAL vs. DISTORT comparison, a cortical activation pattern which resembles more closely the one observed in the NH subjects. Similarly, the cortical activation pattern observed in the bilaterally implanted subjects in the NORMAL vs. MUTE comparison is more similar to the one found in NH children.
Conclusions The results of this study confirm that in NH children the cortical activation in response to musical stimuli is consistent with the Davidson’s approach/withdrawal theory. More importantly, they indicate that unilaterally implanted subjects do not distinguish normal from distorted music in terms of increased/ decreased pleasantness of perceived stimuli. Such a difference may be due both to the peculiar cortical reorganization in prelingually deaf subjects and to an asymmetrical pattern of cortical activation consequential to unilateral CI stimulation. The latter hypothesis seems supported by the finding that sequential, bilateral CI restores a cortical activation pattern which resembles more closely the one observed in the NH group.
References Davidson R.J. 2000. Affective style, psychopathology, and resilience: brain mechanisms and plasticity. American Psychology, 55: 1196–11214. Davidson R.J. 2002. Anxiety and affective style: role of prefrontal cortex and amygdala. Biological Psychiatry 51: 68–80.
Marsella et al.
Neuroelectrical imaging investigation of music perception by children with unilateral and bilateral CIs
Davidson R.J. 2004. What does the prefrontal cortex “do” in affect: perspectives on frontal EEG asymmetry research. Biological Psychology, 67: 219–233. Davidson R.J., Irwin W. 1999. The functional neuroanatomy of emotion and affective style. Trends Cognition Science, 3: 11–21. Galvin J.J.I., Fu Q.J., Nogaki G. 2007. Melodic contour identification by cochlear implant listeners. Ear and Hearing, 28: 302–319. Gfeller K., Christ A., Knutson J.F., Witt S., Murray K.T., Tyler R.S. 2000. Musical backgrounds, listening habits, and aesthetic enjoyment of adult cochlear implant recipients. Journal of American Academy of Audiology, 11: 390–406. Gordon K.A., Wong D.D., Papsin B.C. 2013. Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf. Brain, 136: 1609–1625. Klimesch W. 1999. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Research. Brain Research Review, 29: 169–195.
McDermott H.J. 2004. Music perception with cochlear implants: a review. Trends Amplification, 8: 49–82. Mitani C., Nakata T., Trehub S.E., Kanda Y., Kumagami H., Takasaki K., et al. 2007. Music recognition, music listening, and word recognition by deaf children with cochlear implants. Ear and Hearing, 28(2 Suppl): 29S–33S. Veekmans K., Ressel L., Mueller J., Vischer M., Brockmeier S.J. 2009. Comparison of music perception in bilateral and unilateral cochlear implant users and normal hearing subjects. Audiology and Neurootology, 14: 315–326. Volkova A., Trehub S.E., Schellenberg E.G., Papsin B.C., Gordon K.A. 2013. Children with bilateral cochlear implants identify emotion in speech and music. Cochlear Implants International, 14: 80–91. Vongpaisal T., Trehub S.E., Schellenberg E.G. 2006. Song recognition by children and adolescents with cochlear implants. Journal of Speech Language Hearing Research, 49: 1091–1103.
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